O2 evolution and recovery of the water-oxidizing enzyme

In photosystem II, light-induced water oxidation occurs at the Mn4CaO5 cluster. Here we demonstrate proton releases, dioxygen formation, and substrate water incorporation in response to Mn4CaO5 oxidation in the protein environment, using a quantum mechanical/molecular mechanical approach and molecular dynamics simulations. In S-2, H2O at the W1 site forms a low-barrier H-bond with D1-Asp61. In the S-2-to-S-3 transition, oxidation of OW1H- to O-W1(center dot-), concerted proton transfer from OW1H- to D1-Asp61, and binding of a water molecule Wn-W1 at O-W1(center dot-) are observed. In S-4, Wn-W1 facilitates oxo-oxyl radical coupling between O-W1(center dot-) and corner mu-oxo O4. Deprotonation via D1-Asp61 leads to formation of O-W1=O4. As O-W1=O4 moves away from Mn, H2O at W539 is incorporated into the vacant O4 site of the O-2-evolved Mn4CaO4 cluster, forming a mu-oxo bridge (Mn3-O-W539-Mn4) in an exergonic process. Simultaneously, Wn-W1 is incorporated as W1, recovering the Mn4CaO5 cluster.